Female reproductive fluids ‘rescue’ sperm from phenotypic ageing in an external fertilizer

Female reproductive fluids (FRFs) serve key reproductive functions in sexually reproducing animals, including modifying the way sperm swim and detect eggs, and influencing sperm lifespan. Despite the central role of FRF during fertilization, we know surprisingly little about sperm–FRF interactions under different environmental conditions. Theory suggests that in external fertilizers FRF may ‘rescue’ sperm from ageing effects as they search to fertilize eggs. Here, we test the interaction between these two fundamental properties of the fertilization environment, ejaculate age (i.e. time since ejaculation) and FRF, on a range of functional sperm phenotypes in a broadcast spawning mussel, Mytilus galloprovincialis. We found that the effects of ejaculate age on multivariate sperm motility traits and total sperm motility were altered by FRF, and that longer-lived sperm exhibit stronger, likely more advantageous, responses to FRF after periods of ageing. We also detected significant among-male variation in the relationship between sperm motility traits and ejaculate age; notably, these patterns were only revealed when sperm encountered FRF. Collectively these findings underscore the importance of considering female reproductive physiology when interpreting ageing-related declines in sperm motility, as doing so may expose importance sources of variation in sperm phenotypic plasticity among males and environments.

[1]  J. Fitzpatrick,et al.  Examining the potential for resource‐dependent female reproductive fluid‐sperm interactive effects in a livebearing fish , 2023, Journal of evolutionary biology.

[2]  J. Evans,et al.  Density‐dependent patterns of multivariate selection on sperm motility and morphology in a broadcast spawning mussel , 2022, Ecology and evolution.

[3]  A. Fazeli,et al.  Bovine Follicular Fluid Derived Extracellular Vesicles Modulate the Viability, Capacitation and Acrosome Reaction of Bull Spermatozoa , 2021, Biology.

[4]  J. Evans,et al.  Indirect parental effects on offspring viability by egg-derived fluids in an external fertilizer , 2020, Proceedings of the Royal Society B.

[5]  J. Evans,et al.  Sexual selection after gamete release in broadcast spawning invertebrates , 2020, Philosophical Transactions of the Royal Society B.

[6]  J. Evans,et al.  The role of female reproductive fluid in sperm competition , 2020, Philosophical Transactions of the Royal Society B.

[7]  J. Gadea,et al.  Effect of oviductal fluid on bull sperm functionality and fertility under non-capacitating and capacitating incubation conditions. , 2020, Theriogenology.

[8]  P. Mermillod,et al.  Sperm interactions with the female reproductive tract: A key for successful fertilization in mammals , 2020, Molecular and Cellular Endocrinology.

[9]  J. Evans,et al.  Egg‐induced changes to sperm phenotypes shape patterns of multivariate selection on ejaculates , 2020, Journal of evolutionary biology.

[10]  M. Wolfner,et al.  Post‐ejaculatory modifications to sperm (PEMS) , 2019, Biological reviews of the Cambridge Philosophical Society.

[11]  P. Blier,et al.  Linking paternally inherited mtDNA variants and sperm performance , 2019, Philosophical Transactions of the Royal Society B.

[12]  C. Gasparini,et al.  Effects of ovarian fluid on sperm traits and its implications for cryptic female choice in zebrafish , 2019, Behavioral Ecology.

[13]  Richard Inger,et al.  A brief introduction to mixed effects modelling and multi-model inference in ecology , 2018, PeerJ.

[14]  G. S. van Doorn,et al.  Alternative male morphs solve sperm performance/longevity trade-off in opposite directions , 2018, Science Advances.

[15]  W. J. Kennington,et al.  Multivariate Sexual Selection on Ejaculate Traits under Sperm Competition , 2018, The American Naturalist.

[16]  J. Evans,et al.  Extreme fertilization bias towards freshly inseminated sperm in a species exhibiting prolonged female sperm storage , 2018, Royal Society Open Science.

[17]  D. Levitan Do Sperm Really Compete and Do Eggs Ever Have a Choice? Adult Distribution and Gamete Mixing Influence Sexual Selection, Sexual Conflict, and the Evolution of Gamete Recognition Proteins in the Sea , 2018, The American Naturalist.

[18]  Casper W. Berg,et al.  glmmTMB Balances Speed and Flexibility Among Packages for Zero-inflated Generalized Linear Mixed Modeling , 2017, R J..

[19]  W. J. Kennington,et al.  Egg chemoattractants moderate intraspecific sperm competition , 2017, Evolution letters.

[20]  Steven G. Luke,et al.  Evaluating significance in linear mixed-effects models in R , 2016, Behavior Research Methods.

[21]  D. Scofield,et al.  Haploid selection within a single ejaculate increases offspring fitness , 2017, Proceedings of the National Academy of Sciences.

[22]  Eiji Fujiwara,et al.  Relationships between body size and secondary sexual characters, and sperm characters in male Dolly Varden char (Salvelinus malma) , 2017 .

[23]  J. Cosson,et al.  Ovarian fluid impacts flagellar beating and biomechanical metrics of sperm between alternative reproductive tactics , 2017, Journal of Experimental Biology.

[24]  M. Beekman,et al.  Sexual selection in hermaphrodites, sperm and broadcast spawners, plants and fungi , 2016, Philosophical Transactions of the Royal Society B: Biological Sciences.

[25]  J. Boomsma,et al.  Queen reproductive tract secretions enhance sperm motility in ants , 2016, Biology Letters.

[26]  D. Marshall,et al.  Unravelling anisogamy: egg size and ejaculate size mediate selection on morphology in free-swimming sperm , 2016, Proceedings of the Royal Society B: Biological Sciences.

[27]  Mark J. Brewer,et al.  The relative performance of AIC, AICC and BIC in the presence of unobserved heterogeneity , 2016 .

[28]  Jeffrey A. Riffell,et al.  Sperm chemotaxis promotes individual fertilization success in sea urchins , 2016, Journal of Experimental Biology.

[29]  K. Reinhardt,et al.  An Ecology of Sperm: Sperm Diversification by Natural Selection , 2015 .

[30]  J. Kekäläinen,et al.  Lectin staining and flow cytometry reveals female-induced sperm acrosome reaction and surface carbohydrate reorganization , 2015, Scientific Reports.

[31]  J. Evans,et al.  Multivariate selection drives concordant patterns of pre- and postcopulatory sexual selection in a livebearing fish , 2015, Nature Communications.

[32]  P. Brennan,et al.  Sperm storage: distinguishing selective processes and evaluating criteria. , 2015, Trends in ecology & evolution.

[33]  D. Marshall Environmentally induced (co)variance in sperm and offspring phenotypes as a source of epigenetic effects , 2015, Journal of Experimental Biology.

[34]  J. Fitzpatrick,et al.  Sexual selection and the evolution of sperm quality. , 2014, Molecular human reproduction.

[35]  G. Parker The sexual cascade and the rise of pre-ejaculatory (Darwinian) sexual selection, sex roles, and sexual conflict. , 2014, Cold Spring Harbor perspectives in biology.

[36]  D. Bates,et al.  Fitting Linear Mixed-Effects Models Using lme4 , 2014, 1406.5823.

[37]  J. Evans,et al.  Chemically moderated gamete preferences predict offspring fitness in a broadcast spawning invertebrate , 2014, Proceedings of the Royal Society B: Biological Sciences.

[38]  I. Fleming,et al.  Sperm plasticity to seawater temperatures in Atlantic cod Gadus morhua is affected more by population origin than individual environmental exposure , 2014 .

[39]  J. Crimaldi,et al.  The physics of broadcast spawning in benthic invertebrates. , 2014, Annual review of marine science.

[40]  J. Evans,et al.  Sexual Selection and the Evolution of Egg-Sperm Interactions in Broadcast-Spawning Invertebrates , 2013, The Biological Bulletin.

[41]  M. Gomendio,et al.  POSTCOPULATORY SEXUAL SELECTION INCREASES ATP CONTENT IN RODENT SPERMATOZOA , 2013, Evolution; international journal of organic evolution.

[42]  J. Evans,et al.  Ovarian Fluid Mediates the Temporal Decline in Sperm Viability in a Fish with Sperm Storage , 2013, PloS one.

[43]  D. Marshall,et al.  THE MAINTENANCE OF SPERM VARIABILITY: CONTEXT‐DEPENDENT SELECTION ON SPERM MORPHOLOGY IN A BROADCAST SPAWNING INVERTEBRATE , 2012, Evolution; international journal of organic evolution.

[44]  D. T. R. Moreau,et al.  Stressful environments induce novel phenotypic variation: hierarchical reaction norms for sperm performance of a pervasive invader , 2012, Ecology and evolution.

[45]  J. Evans,et al.  Assessing the potential for egg chemoattractants to mediate sexual selection in a broadcast spawning marine invertebrate , 2012, Proceedings of the Royal Society B: Biological Sciences.

[46]  L. Simmons,et al.  COMPLEX PATTERNS OF MULTIVARIATE SELECTION ON THE EJACULATE OF A BROADCAST SPAWNING MARINE INVERTEBRATE , 2012, Evolution; international journal of organic evolution.

[47]  K. Ota,et al.  Sperm phenotypic plasticity in a cichlid: a territorial male's counterstrategy to spawning takeover , 2010 .

[48]  E. Trippel,et al.  Thermal reaction norms in sperm performance of Atlantic cod (Gadus morhua). , 2010 .

[49]  J. Boomsma,et al.  Honey bee males and queens use glandular secretions to enhance sperm viability before and after storage. , 2009, Journal of insect physiology.

[50]  D. Hanley,et al.  Secondary sexual characters and sperm traits in coho salmon Oncorhynchus kisutch. , 2009, Journal of fish biology.

[51]  L. Simmons,et al.  Sperm competition: linking form to function , 2008, BMC Evolutionary Biology.

[52]  Manabu Yoshida,et al.  Control of sperm motility and fertility: Diverse factors and common mechanisms , 2008, Cellular and Molecular Life Sciences.

[53]  Sébastien Lê,et al.  FactoMineR: An R Package for Multivariate Analysis , 2008 .

[54]  M. Bonsall,et al.  The evolutionary ecology of pre- and post-meiotic sperm senescence. , 2008, Trends in ecology & evolution.

[55]  K. Reinhardt Evolutionary Consequences of Sperm Cell Aging , 2007, The Quarterly Review of Biology.

[56]  R. Deana,et al.  Variation pattern of sperm quality traits in two gobies with alternative mating tactics , 2007 .

[57]  R. Ingermann,et al.  Development of a novel CASA system based on open source software for characterization of zebrafish sperm motility parameters. , 2007, Theriogenology.

[58]  Shane A. Richards,et al.  TESTING ECOLOGICAL THEORY USING THE INFORMATION‐THEORETIC APPROACH: EXAMPLES AND CAUTIONARY RESULTS , 2005 .

[59]  J. Riffell,et al.  The ecological and evolutionary consequences of sperm chemoattraction. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[60]  R. Montgomerie,et al.  Sperm swimming speed and energetics vary with sperm competition risk in bluegill (Lepomis macrochirus) , 2004, Behavioral Ecology and Sociobiology.

[61]  D. Kime,et al.  Long lasting stickleback sperm; is ovarian fluid a key to success in fresh water? , 2003 .

[62]  G. Parker,et al.  Relationships between sperm morphometry and sperm motility in the Atlantic salmon , 2002 .

[63]  R. Montgomerie,et al.  Ovarian fluid enhances sperm movement in Arctic charr , 2002 .

[64]  D. Levitan Sperm velocity and longevity trade off each other and influence fertilization in the sea urchin Lytechinus variegatus , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[65]  M. Kenward,et al.  Small sample inference for fixed effects from restricted maximum likelihood. , 1997, Biometrics.

[66]  J. Havenhand,et al.  Chemical Mediation of Sperm Activity and Longevity in the Solitary Ascidians Ciona intestinalis and Ascidiella aspersa. , 1996, The Biological bulletin.

[67]  J. Benzie,et al.  Small-Scale Dispersion of Eggs and Sperm of the Crown-of-Thorns Starfish (Acanthaster planci) in a Shallow Coral Reef Habitat. , 1994, The Biological bulletin.

[68]  M. Sewell,et al.  Kinetics of Fertilization in the Sea Urchin Strongylocentrotus franciscanus: Interaction of Gamete Dilution, Age, and Contact Time. , 1991, The Biological bulletin.

[69]  Mark F Shibata,et al.  Consequences of Surf-Zone Turbulence for Settlement and External Fertilization , 1989, The American Naturalist.

[70]  R. Gorsuch Exploratory Factor Analysis , 1988 .

[71]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[72]  J. Cummins Sperm motility and energetics , 2009 .

[73]  R. Montgomerie,et al.  Chemical composition of seminal and ovarian fluids of chinook salmon (Oncorhynchus tshawytscha) and their effects on sperm motility traits. , 2009, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[74]  P. Borsa,et al.  Genetic relationships of Mytilus galloprovincialis Lamarck populations worldwide: evidence from nuclear-DNA markers , 2000, Geological Society, London, Special Publications.

[75]  M. Eisenbach Sperm chemotaxis. , 1999, Reviews of reproduction.

[76]  D. Levitan 6 – Sperm Limitation, Gamete Competition, and Sexual Selection in External Fertilizers , 1998 .

[77]  J. Young Echinodermata , 1871, Transactions of the Glasgow Geological Society.